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The Blood Supply of The Large Intestine: January 2008
The Blood Supply of The Large Intestine: January 2008
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Abstract
The aim of the study was to describe and depict the spatial arrangement of the colon microcirculatory bed as a
whole. Various parts of the large intestine and terminal ileum were harvested from either cadaver or section
material or gained peroperatively. Samples were then injected with India ink or methylmetacrylate Mercox resin
for microdissection and corrosion casting for scanning electron microscopy. The results showed that extramural
vasa recta ramified to form the subserous plexus, some of them passing underneath the colon taeniae. Branches
of both short and long vasa recta merged in the colon wall, pierced the muscular layer and spread out as the
submucous plexus, which extended throughout the whole intestine without any interruption. The muscular
layer received blood via both the centrifugal branches of the submucous plexus and the minor branches sent
off by the subserous plexus. The mucosa was supplied by the mucous plexus, which sent capillaries into the
walls of intestinal glands. The hexagonal arrangement of the intestinal glands reflected their vascular bed. All
three presumptive critical points are only gross anatomical points of no physiological relevance in healthy indi-
viduals. Neither microscopic weak points nor regional differences were proven within the wall of the whole
large intestine. The corrosion casts showed a huge density of capillaries under the mucosa of the large intes-
tine. A regular hexagonal pattern of the vascular bed on the inner surface was revealed. No microvascular criti-
cal point proofs were confirmed and a correlation model to various pathological states was created.
Key words injection; large intestine; microcirculation; scanning electron microscopy.
Fig. 5 The external view of the surface of the vascular bed of the
large intestine in the scanning electron microscope. Corrosion cast.
Bar: 2 mm. VR1, VR2, adjacent vasa recta.
The branches derived from this plexus and from all vessels
passing the muscular layer are called the interfascicular
branches (rami interfasciculares). Their diameter ranges
from 10 to 20 lm and they run rectilinearly between the
muscle fascicles which they supply. There are rich mutual
anastomoses. Finally, they send the fascicular branches
(rami fasciculares), which are 10–15 lm in diameter, into
the muscle fascicles perpendicularly to their longitudinal
axis. Their terminal branches are the precapillary arterioles
anastomosing with each other and forming a terminal arte-
riolar network giving rise to the capillary bed of the muscu-
lar fascicle (see Figs 3, 4 and 6).
Fig. 8 The detail of the longitudinal section of the vascular bed of the The entire thickness of the mucosa is regularly juxtaposed
large intestine in the scanning electron microscope. Corrosion cast. by intestinal glands (glandulae intestinales; Lieberkühn’s
Bar: 200 lm. Mu, tunica mucosa; Sm, tunica submucosa; C, crypts). The upper ends of the glands open into the intesti-
glandulae intestinales = Lieberkühn’s crypts; a, artefacts (extravasate). nal lumen and the bases reach as deep as the muscularis
mucosae. The mucous plexus resembles a mosaic because of
its regular dimensions and shape. The diameter of its vessels
lar and rectilinear direction through the circular muscle ranges from 25 to 30 lm. The mucous plexus is fed by the
layer (750–1000 lm). They terminate in the intermuscular mucosal branches from the submucous plexus. They run
plexus, which is parallel to the longitudinal axis of the intes- perpendicularly to the longitudinal axis of the intestine.
tine. Finally, the long branches (rami musculares recurrentes Due to the presence of folds on the mucosal surface, their
longi) have the same orientation as the middle branches course is variable and they can be classified as long and
but reach as far as the muscular bundles of the taeniae short (see Figs 6–8).
(longitudinal muscular layer). Some may even join the sub- The short mucous branches (rami mucosi breves) run to
serous plexus. During their course, they send off branches the segments of mucosa located between two semilunar
for both muscular layers and for the intermuscular plexus, folds. They originate from the adjacent submucous plexus
their length ranging from 1500 to 2000 lm. There are fre- and send off two to four collateral branches. Their length
quent anastomoses between collateral and terminal ranges from 500 to 1000 lm. The long mucous branches
branches of all types of the recurrent muscular branches. (rami mucosi longi) run in the mucosa of the semilunar
The second source of the arterial blood vessels, although folds. Their course is more rectilinear and sometimes slightly
less numerous in branches and less voluminous, is provided flexed. The long mucous branches range in length from 2
by arteries issued centripetally from the subserous plexus to 5 mm. Each branch bifurcates at a variable distance from
(rami musculares plexus subserosi). These can be classified the lumen into two branches of the first order (15 lm in
as long and muscular branches. They originate from either diameter). These branches then send off two or three more
the vasa recta or from their collaterals and anastomoses. branches of second order, respectively. All of these collater-
Although not as significant as the recurrent muscular als successively send the precapillary arterioles (10 lm in
branches from the submucous plexus, these branches con- diamater). The arterioles coil round the bases and bodies of
tribute considerably to the arterial blood supply of all three the intestinal glands and descend as far as the furthermost
taeniae. Their diameter is approximately 25 lm. luminal surface. Some of the arterioles run a straight course
The short muscular branches enter the taeniae (longitudi- but the majority form waves and intermingle with each
nal muscular layer) running perpendicularly to the longitu- other, sending off capillaries. A dense network of capillaries
dinal axis of the intestine and supply them. Some terminal covers the glands, which are embedded in a vascular cush-
branches reach the intermuscularis plexus, being 200 lm ion (see Fig. 8).
long (or 400 lm via the taenia) and helping to feed it. The The luminal surface is covered by capillaries. They change
long muscular branches pass through the longitudinal mus- their direction from perpendicular to horizontal and then
cular layer and send off some nourishing branches. They they turn back and run deep to join a venule. They may also
then join or pass the intermuscular plexus within the inter- curve along the circular opening brim of the gland orifice,
muscular space and terminate in the circular muscular layer. encircling it like rods of a wreath (see Fig. 9).
Their length is usually between 750 and 1500 lm. In rare The wreath-like structures are formed by one to five cap-
cases, they may even reach the submucous plexus and con- illaries and have various widths. The capillaries anastomose
tribute to its blood supply. with each other to encircle the circumference of the gland
Discussion
Resin corrosion injections are the most suitable technique
to depict and study the arrangement of blood vessels in the
intestinal wall at both the macroscopic and microscopic
level (Shikata & Shida, 1985; Christofferson & Nilsson, 1988;
Krstić, 1991; Aharinejad et al. 1992; Hossler, 1998). Our stud-
ies confirm this. As for the microcirculatory bed of the wall
of the large intestine, there are several studies reporting
Fig. 10 The overview of the vascular bed luminal surface of the large
the successful application of this technique in animals
intestine in the scanning electron microscope. Corrosion cast. Bar:
200 lm. Hexagons of the bee honeycomb arrangement of glandulae (Shikata & Shida, 1985; Browning & Gannon, 1986; Christ-
intestinales. offerson & Nilsson, 1988; Krstić, 1991; Aharinejad et al.
1992; Skinner et al. 1995; Hossler, 1998; Sangiorgi et al.
orifice. The length of each individual capillary is different, 2007) but only few articles concerning the application in
ranging from a narrow spot, enabling the capillary to humans (Gannon et al. 1984; Sun et al. 1992; Skinner et al.
change the ascending course into the descending course, to 1995; Araki et al. 1996; Fait et al. 1998). In animals, the prin-
one-half of the gland orifice circumference (see Fig. 10). cipal study was published by Shikata & Shida (1985). They
Some capillaries connect adjacent wreathes of vessels, usu- applied this technique in the experimental study of colon
ally in more anastomosing sites. This mosaic (carpet) is iden- anastomosis in healing after the stapler operation using
tical to the SEM picture of the normally-shaped intestinal instruments of various origins in dogs. Gannon et al. (1984)
mucosa. The outline of the glands is maintained mainly by carried out an experiment involving vascular injections fol-
the dense network of the superficially laid capillaries form- lowed by in-vivo microscopy of the laboratory rat large
intestine. Details of the morphological relationship of indi- ularly to the longitudinal axis of the intestine, thus forming
vidual plexuses to the corresponding intestinal wall layers the second striation. Such an arrangement, first described
and the level of their location were reported by Bernardes in detail by Wolfram-Gabel et al. (1984), resembles that
& Patrı́cio (2004), Boulter & Parks (1960), Goerttler (1932), reported by Szyika (1976) in the jejunum and ileum. Apart
Horstmann (1943), Ohtsuka et al. (1988), Wolfram-Gabel & from nourishing the subserous layer, the main purpose of
Maillot (1981) and Wolfram-Gabel et al. (1982, 1983, 1984, the vasa recta is to penetrate the muscular layer. There are
1986). To compare the data of various segments of the gas- several terminal branches penetrating deep into the wall to
trointestinal tube, see studies by Wolfram-Gabel et al. the submucous layer (Griffiths, 1961 reported four main
(1984, 1986); the duodenum was scrutinized by Szyika sites without any detailed data).
(1976) and Wolfram-Gabel et al. (1982), and the small intes- Ernst (1851) observed that the long vasa recta penetrat-
tine and stomach by Barclay & Bentley (1949). ing the muscular layer send off branches supplying it. Later,
The vascular bed of the large intestine, as described Heller (1872) added the description of the blood supply of
above, resembles a similar arrangement of the intramural the muscular layer directly from the subserous plexus (for
arteries in the stomach (Barclay & Bentley, 1949; Gannon more details, see Hou-Jensen, 1931 and Wolf-Heidegger,
et al. 1984) and small intestine (Szyika, 1976). It also reflects 1942). The intermuscular plexus itself is interposed between
the vascular arrangement in the striated muscle, which was the internal (circular) and external (longitudinal) muscular
described by Saunders et al. (1957) as ‘macromesh’ with a layers (arranged in the taeniae in the majority of the large
finer plexus within it called the ‘micromesh’. In the large intestine) in the intermuscular space. It is rather thin but it
intestine, the term ‘micromesh’ can be applied to the supplies the thickest layer of the large intestinal wall. This is
mucous plexus between the epithelium of the mucosa and the reason why there are accessory vessels directly derived
the submucosa. The rich mucous vascular bed was termed from the adjacent plexuses (subserous and submucous).
the ‘carpet’ by Brockis & Moffat (1958) who discovered the These vessels contribute to the supply of the muscle bundles
similarity of the loops around the intestinal glands with the and fibres without interpolating in any further plexus. The
carpet pattern. plexus helps to hold both muscular layers in place. The long
As for the terminology, we followed the terms proposed recurrent muscular branches have the same course as the
by Wolfram-Gabel & Maillot (1981) and Wolfram-Gabel middle branches but reach as far as the longitudinal muscu-
et al. (1982, 1983, 1984, 1986) and added the Latin terms to lar layer (taeniae). Some even join the subserous plexus, as
all of the branches and plexus described (in brackets using stated by Wolfram-Gabel et al. (1984). The second source of
italics) because the Terminologia Anatomica (1998) and the arterial blood vessels, although less frequent in
Terminologia Histologica (2007) do not include any terms branches and less voluminous, is provided by arteries issued
concerning the microcirculatory bed of the intestine (FCAT by the subserous plexus centripetally. Wolfram-Gabel et al.
1998; FICAT, 2008). (1984) called them the ‘arteriae musculares’ but we recom-
As early as 1736, Albinus described the branching of the mend the term muscular branches from subserous plexus
intramural vessels in the intestinal wall but his study was (rami musculares plexus subserosi). As for the mucous
limited to the small intestine. This was proven by the trans- plexus, our results of the diameter of the intestinal gland
lation of his thesis (Albinus, 1736; Kachlik, 2006; Kachlik & orifices (varying from 60 to 90 lm) are similar to those
Hoch, 2008). Bourgery (1839) described the subserous plexus reported by Wolfram-Gabel et al. (1983) (80–100 lm).
as the principal plexus issuing arteries for the deeper layers Al-Fallouji (1984) was the first to emphasize that there
of the intestinal wall. Mellière (1927) assumed the vasa are no regional differences in the arrangement of the intra-
recta to be branches from the marginal artery, opening out mural plexuses of the large intestine. Any segment of the
in the subserous connective tissue into a plexus nourishing large intestine can be used as the terminal end for a postre-
all deeper layers. section anastomosis. There is no morphological background
There is extensive branching of the subserous arteries, for the development of ischaemic consequences after the
especially in anastomotic branches that are rich in the subs- anastomosis of two segments of the large intestine follow-
erous layer and can be divided into anastomoses of the first ing resection. Rather, the factors of primary importance
and second order, respectively. The first-order anastomoses include: the calibre of the colon lumen, width of the colon
are situated either between two collateral branches, wall and the mobility of the colon segment. The danger of
between two terminal branches or between the collateral ischaemia is due to the extensive traction of the mesocolon
and terminal branch of the adjacent vasa recta. Their diam- or the newly anastomosed large intestine.
eter is approximately 50 lm and they are arranged in a reg- The existence of the continuous intramural plexuses
ular network with distances between adjacent vessels from within the whole length of the small and large intestine
1.4 to 2.0 mm. This creates an impression of the continuous allows us to confirm the theory of a compact intestinal intra-
and regular striation. The second-order anastomoses (being mural vascular canal. Such a connection is like one huge
of the same dimensions) are branches of the previous level anastomosis that can replace the blood supply of one source
of anastomoses, situated mostly transversely and perpendic- artery if some disruption in flow occurs. A blockage due to
either iatrogenic (ligation) or pathological (embolization, colon is almost single-layered. He speculated that the capil-
thrombosis, obturation or arteriosclerosis) causes can be lary network of the ascending colon is closely related to the
compensated in varying degrees by the anastomoses, which greater degree of water absorption and electrolyte trans-
allow a change in the direction of blood flow. Especially in port activities compared with those of the sigmoid colon.
the rectum, the theory of the inverted blood flow from the
middle and inferior rectal artery to the network of the supe-
Concluding remarks
rior rectal artery, and even more orally, was suggested by
McGregor (1957) and Sunderland (1942). This theory is piv- This article brings together thorough and comprehensive
otal for the denial of the physiological function of the critical information on the arrangement of the blood supply to the
points. These points exist as places of the interrupted blood large intestine wall. All vascular plexuses are connected in a
supply. In certain cases, the macroscopically visible anasto- long channel running through the whole length of the
moses may be absent. In the otherwise healthy and unaf- intestine. If necessary, it can serve as a huge collateral. This
fected patient, they have no physiological function. collateral is sufficient only in an otherwise non-afflicted
However, in cases of any pathological affliction or embryo- intestine (without developmental defect, immune, vascular
logical discrepancy [e.g. in infant necrotizing colitis, arterio- or connective tissue diseases, etc.). It presents a model that
sclerosis (abdominal angina), venous thrombosis and states can serve as a background for other studies concerning the
with disrupted haemocoagulation], these points indicate changes of the large intestine wall blood supply in various
predisposed sites of vulnerability. pathological states, such as colorectal cancer, inflammatory
The architecture of the capillary network in the large bowel disease, especially Crohn’s disease, etc.
intestine segments was qualitatively described by Aharine-
jad & Lametschwandtner (1992) in rats and guinea pigs, by
Acknowledgements
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et al. (1992) in normal tissue, transitional mucosa and ade- 103 ⁄ 2004 ⁄ C. Special thanks to Prof. Alois Lametschwandtner
nocarcinoma, by Skinner et al. (1995) comparing rat and (Department of Organismic Biology, Vascular and Muscle
Research Unit, University of Salzburg, Austria) for the use of the
human colon and by Araki et al. (1996) and Fait et al.
SEM laboratory.
(1998). Interestingly, comparisons to the microvascular
architecture of the small intestine revealed some differ-
ences. Skinner et al. (1995) presented different types of Author contributions
microvascular architecture within the individual villi. He dis-
D.K. – substantial contributions to the conception and design,
cerned a fountain-like arrangement, in which the arterioles performance of the injections, corrosion casting, acquisition of
reach the top of the villus without branching (‘fountain- data or analysis and interpretation of data. V.B. – substantial
type’), a deeply interconnected type (‘step ladder’) and a contributions to the conception and design, performance of the
‘tuft-type’. Unfortunately, this classification cannot be injections, corrosion casting, acquisition of data or analysis and
applied to the large intestine. Browning & Gannon (1986) interpretation of data. J.S. – senior author, final approval of the
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